Control of neuronal excitability by NMDA-type glutamate receptors in early developing binaural auditory neurons

Journal of Physiology

Volumn 590, Issue 19, 2012, Pages 4801-4818

  Sanchez, Jason Tait ^a   Seidl, Armin H ^a   Rubel, Edwin W ^a   Barria, Andres ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; VOLTAGE GATED POTASSIUM CHANNEL;

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; DENDRITE; EVOKED BRAIN STEM AUDITORY RESPONSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; THALAMUS INTRALAMINAR NUCLEUS;

ACTION POTENTIALS; ANIMALS; BRAIN STEM; CHICK EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; NEURONS; POTASSIUM CHANNELS, VOLTAGE-GATED; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84866849853     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.228734     Document Type: Article

References (66)

1. Ashida G, Abe K, Funabiki K & Konishi M (2007). Passive soma facilitates submillisecond coincidence detection in the owl's auditory system. J Neurophysiol 97, 2267-2282.
2. Barnes-Davies M, Barker MC, Osmani F & Forsythe ID (2004). Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19, 325-333.
3. Bartlett EL & Smith PH (2002). Effects of paired-pulse and repetitive stimulation on neurons in the rat medial geniculate body. Neuroscience 113, 957-974.
4. Born DE, Durham D & Rubel EW (1991). Afferent influences on brainstem auditory nuclei of the chick: nucleus magnocellularis neuronal activity following cochlea removal. Brain Res 557, 37-47.
5. + conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15, 8011-8022.
6. Burger RM & Rubel EW (2008). Encoding of interaural timing for binaural hearing. In The Senses: A Comprehensive Review, vol. 3, Audition, ed. Dallos P & Oertel D, pp. 613-630. Academic Press, San Diego.
7. Burnashev N, Zhou Z, Neher E & Sakmann B (1995). Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J Physiol 485, 403-418.
8. Carr CE & Konishi M (1990). A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10, 3227-3246.
9. Cook DL, Schwindt PC, Grande LA & Spain WJ (2003). Synaptic depression in the localization of sound. Nature 421, 66-70.
10. Erreger K, Dravid SM, Banke TG, Wyllie DJ & Traynelis SF (2005). Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signaling profiles. J Physiol 563, 345-358.
11. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR & Monyer H (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17, 2469-2476.
12. Futai K, Okada M, Matsuyama K & Takahashi T (2001). High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21, 3342-3349.
13. Gambrill AC, Storey GP & Barria A (2011). Dynamic regulation of NMDA receptor transmission. J Neurophysiol 105, 162-171.
14. Gan L & Kaczmarek LK (1998). When, where, and how much? Expression of the Kv3.1 potassium channel in high-frequency firing neurons. J Neurobiol 37, 69-79.
15. Gao H & Lu Y (2008). Early development of intrinsic and synaptic properties of chicken nucleus laminaris neurons. Neuroscience 153, 131-143.
16. Hestrin S (1992). Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357, 686-689.
17. Hogsden JL & Dringenberg HC (2009). NR2B subunit-dependent long-term potentiation enhancement in the rat cortical auditory system in vivo following masking of patterned auditory input by white noise exposure during early postnatal life. Eur J Neurosci 30, 376-384.
18. Howard MA & Rubel EW (2010). Dynamic spike thresholds during synaptic integration preserve and enhance temporal response properties in the avian cochlear nucleus. J Neurosci 30, 12063-12074.
19. Johnston J, Forsythe ID & Kopp-Scheinpflug C (2010). Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588, 3187-3200.
20. Joseph AW & Hyson RL (1993). Coincidence detection by binaural neurons in the chick brain stem. J Neurophysiol 69, 1197-1211.
21. Kuba H (2010). Plasticity at the axon initial segment. Commun Intgr Biol 6, 597-598.
22. Kuba H, Ishii TM & Ohmori H (2006). Axonal site of spike initiation enhances auditory coincidence detection. Nature 444, 1069-1072.
23. Kuba H, Koyano K & Ohmori H (2002). Synaptic depression improves coincidence detection in the nucleus laminaris in brainstem slices of the chick embryo. Eur J Neurosci 15, 984-990.
24. + channel distribution at the axon initial segment. Nature 465, 1075-1078.
25. Kuba H, Yamada R, Fukui I & Ohmori H (2005). Tonotopic specialization of auditory coincidence detection in nucleus laminaris of the chick. J Neurosci 25, 1924-1934.
26. Kuba H, Yamada R & Ohmori H (2003). Evaluation of the limiting acuity of coincidence detection in nucleus laminaris of the chicken. J Physiol 552, 611-620.
27. Lippe WR (1994). Rhythmic spontaneous activity in the developing auditory brainstem. J Neurosci 3, 1486-1495.
28. Lu Y, Harris JA & Rubel EW (2007). Development of spontaneous miniature EPSCs in mouse AVCN neurons during a critical period of afferent-dependent neuron survival. J Neurophysiol 97, 635-646.
29. Lu Y, Monsivais P, Tempel BL & Rubel EW (2004). Activity-dependent regulation of the potassium channel subunits Kv1.1 and Kv3.1. J Comp Neurol 470, 93-106.
30. v1 channels. Nat Neurosci 13, 601-609.
31. Oertel D (1991). The role of intrinsic neuronal properties in the encoding of auditory information in the cochlear nuclei. Curr Opin Neurobiol 1, 221-228.
32. Oertel D (1997). Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19, 959-962.
33. Otis TS, Wu YC & Trussell LO (1996). Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16, 1634-1644.
34. Parameshwaran-Iyer S, Carr CE & Perney TM (2003). Localization of KCNC1 (Kv3.1) potassium channel subunits in the avian auditory nucleus magnocellularis and nucleus laminaris during development. J Neurobiol 55, 165-178.
35. Patneau DK & Mayer ML (1990). Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10, 2385-2399.
36. Pena JL, Viete S, Funabiki K, Saberi K & Konishi M (2001). Cochlear and neural delays for coincidence detection in owls. J Neurosci 21, 9455-9459.
37. Pliss L, Yang H & Xu-Friedman MA (2009). Context-dependent effects of NMDA receptors on precise timing information at the endbulb of held in the cochlear nucleus. J Neurophysiol 102, 2627-2637.
38. Porres CP, Meyer EM, Grothe B & Felmy F (2011). NMDA currents modulate the synaptic input-output functions of neurons in the dorsal nucleus of the lateral lemniscus in Mongolian gerbils. J Neurosci 31, 4511-4523.
39. Raman IM, Zhang S & Trussell LO (1994). Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J Neurosci 14, 4998-5010.
40. Ravindranathan A, Donevan SD, Sugden SG, Greig A, Rao MS & Parks TN (2000). Contrasting molecular composition and channel properties of AMPA receptors on chick auditory and brainstem motor neurons. J Physiol 523, 667-684.
41. Reyes AD, Rubel EW & Spain WJ (1994). Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14, 5352-5364.
42. Reyes AD, Rubel EW & Spain WJ (1996). In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J Neurosci 16, 993-1007.
43. Rothman JS & Manis PB (2003). Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J Neurophysiol 89, 3083-3096.
44. Rubel EW & Parks TN (1988). Organization and development of the avian brain-stem auditory system. In Brain Function, ed. Edelman GM, Einar Gall W & Maxwell Cowan W, pp. 3-92. John Wiley & Sons, New York.
45. Sanchez JT, Gans D & Wenstrup JJ (2007). Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus. J Neurosci 27, 1954-1963.
46. Sanchez JT, Wang Y, Rubel EW & Barria A (2010). Development of glutamatergic synaptic transmission in binaural auditory neurons. J Neurophysiol 104, 1774-1789.
47. Scott LL, Mathews PJ, Golding NL (2005). Post hearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J Neurosci 25, 7887-7895.
48. Seidl AH, Rubel EW & Harris DM (2010). Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30, 70-80.
49. Sivaramakrishnan S & Oliver DL (2006). Neuronal responses to lemniscal stimulation in laminar brain slices of the inferior colliculus. J Assoc Res Otolaryngol 7, 1-14.
50. Slee SJ, Higgs MH, Fairhall AL & Spain WJ (2010). Tonotopic tuning in a sound localization circuit. J Neurophysiol 103, 2857-2875.
51. 2+] signaling in individual hippocampal dendritic spines. J Neurosci 25, 6037-6046.
52. Sorensen SA & Rubel EW (2006). The level and integrity of synaptic input regulates dendrite structure. J Neurosci 26, 1539-1550.
53. Steinert JR, Postlethwaite M, Jordan MD, Chernova T, Robinson SW & Forsythe ID (2010). NMDAR-mediated EPSCs are maintained and accelerate in time course during maturation of mouse and rat auditory brainstem in vitro. J Physiol 588, 447-463.
54. Stevens CF & Wang Y (1995). Facilitation and depression at single central synapses. Neuron 14, 795-802.
55. Stocca G & Vicini S (1998). Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 507, 13-24.
56. Sung MJ, Ahn HS, Hahn SJ & Choi BH (2008). Open channel block of Kv3.1 currents by fluoxetine. J Pharmacol Sci 106, 38-45.
57. Tang YZ & Carr CE (2004). Development of NMDA R1 expression in chicken auditory brainstem. Hear Res 191, 79-89.
58. Tang YZ & Carr CE (2007). Development of N-methyl-D-aspartate receptor subunits in avian auditory brainstem. J Comp Neurol 502, 400-413.
59. Tang ZQ, Dinh EH, Shi W & Lu Y (2011). Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism. J Neurosci 31, 6121-6131.
60. Taschenberger H, von Gersdorff H (2000). Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20, 9162-9173.
61. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ & Dingledine R (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
62. Trussell L (1998). Control of time course of glutamatergic synaptic currents. Prog Brain Res 116, 59-69.
63. Trussell LO (1999). Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61, 477-496.
64. Wang LY, Gan L, Forsythe ID & Kaczmarek LK (1998). Contribution of the Kv3.1 potassium channel to high frequency firing in mouse auditory neurones. J Physiol 509, 183-194.
65. A receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J Neurosci 24, 4625-4634.
66. Yashiro K & Philpot BD (2008). Regulation of NMDA-R subunit expression and its implication for LTD, LTP and metaplasticity. Neuropharmacol 55, 1081-1094.